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Fruit fly surveillance in Togo (West Africa): state of diversity and prevalence of

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Article  in  International Journal of Tropical Insect Science · August 2021

DOI: 10.1007/s42690-021-00504-9

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International Journal of Tropical Insect Science
https://doi.org/10.1007/s42690-021-00504-9

ORIGINAL RESEARCH ARTICLE

Fruit fly surveillance in Togo (West Africa): state of diversity

and prevalence of species
Komina Amevoin1   · L. K. Agboyi2 · M. Gomina1 · K. Kounoutchi3 · K. H. Bassimbako3 · M. Djatoite3 · A. V. Dawonou3 ·
A. Tagba3

Received: 18 November 2020 / Accepted: 11 March 2021

© The Author(s) 2021

Abstract
The production and marketing of fruits, especially mango, in sub-Saharan Africa are threatened by fruit flies (Diptera: Teph-
ritidae). This baseline study analysed the biodiversity of fruit fly species, in mango orchards, in different ecological zones
of Togo. Traps used to monitor the flies in the orchards consisted of dry baits, made from four types of parapheromones
specific to the males of different species. Forty species of fruit flies were identified in the mango orchards in Togo. The
most common species were Bactrocera dorsalis (Hendel), Ceratitis cosyra (Walker), Ceratitis fasciventris (Bezzi), Ceratitis
capitata (Wiedemann), Ceratitis bremii Guérin-Méneville, Dacus bivittatus (Bigot), Dacus humeralis (Bezzi), Dacus punc-
tatifrons Karsch and Zeugodacus cucurbitae (Coquillett). The invasive B. dorsalis and the endogenous species, C. cosyra
were dominant in the mango producing areas of Togo because their prevalence were very high (B. dorsalis: 2.1 ≤ flies per
trap per day (FTD) ≤ 472.2; C. cosyra: 0.34 ≤ FTD ≤ 97.28). There was no area free from fruit flies in Togo during the study.
These results constitute an essential reference in the future evaluation of the effectiveness of any control activities initiated
in Togo against fruit flies.

Keywords  Surveillance · Tephritidae · Bactrocera dorsalis · Ceratitis cosyra · Invasive exotic species · Togo

Introduction good quality fruits and vegetables because of their nutri-

The consumption of fruits and vegetables is at the core of
a healthy diet (Amiot-Carlin et al. 2007; Griep et al. 2010;
Zhang et al. 2011). Fruits and legumes are an important
source of water, fiber, vitamins (A, B9, C, E), minerals
(Calcium, phosphorus, Zinc, Iron, Selenium, Magnesium)
and antioxidants necessary for the proper functioning of the
body (Amiot-Carlin et al. 2007). The demand for healthy
vegetable and fruit products is increasing in West Africa
where consumers are increasingly purchasing expensive,
Komina Amevoin: Deceased
* L. K. Agboyi
l.agboyi@cabi.org
1
Laboratoire D’Entomologie Appliquée, Faculté Des
Sciences, Université de Lomé, 01 BP 1515 Lomé 01, Lomé,
Togo
2
CABI, P.O. Box CT 8630, GA 0376800 Cantonments, Accra,
Ghana
3
Direction de La Protection Des Végétaux, Ministère de
L’Agriculture, de La Production Animale Et Halieutique, BP
1347, Lomé, Togo
tional importance (FAO and BAD 2015). Moreover, sev-
eral exploratory and epidemiological studies have shown
that high consumption of vegetables and fruits reduces the
risk of cardiovascular diseases and the occurrence of some
cancerous and other chronic diseases (Zhang et al. 2011;
He et al. 2007; CIRAD 2009). To respond in part to the
growing urban demand for fruits and vegetables, especially
the diversification of diet as a source of welfare, West Afri-
can countries are developing their horticultural sectors and
production has more than doubled in 26 years, increasing
from 14,403,034 tons in 1980 to 32,668,682 tons in 2008,
with average growth rates of 1% and 1.7% for fruits and
vegetables, respectively (FARM 2008). The production and
trade in fruits and vegetables is an important income source
for countries in general and those of sub-Saharan Africa in
particular. In Togo, fruit and vegetable production is esti-
mated at around 560,000 tons in 2017 (InterFaxPress 2019).
Apart from their importance in food security, the production
and trade in fruits and vegetables is an important income
source for sub-Saharan African countries. Indeed, in 2017,
the horticultural sector contributed an income of 4.5 billion

13
Vol.:(0123456789)

FCFA to the national economy of Togo, with 30,265 tons
exported (Vert Togo 2019). Given its importance, the fruit
and vegetable sector is one of the key agricultural sectors
targeted for promotion in Togo’s National Development
Plan (PND). Of those targeted, mango, Mangifera indica
L. (Anacardiaceae) is one of the important commercial
fruit tree crops in the world (Akotsen-Mensah et al. 2017).
According to theses authors, mango grows in the tropical
and subtropical climates, making it second to citrus in terms
of production. It continues to be an important tropical fruit
for Sub-Saharan African economies and serving as a major
source of nutrition for the rural population, playing a major
role in poverty reduction as well as being a potential export
product (Vayssieres et al. 2008). In Togo, mango grows in
the five economic regions of the country on approximately
1,523 hectares with a production of 340,000 tons and a yield
of 3.7 tons per hectare (InterFaxPress 2019; MAEDR 2020).
Apart from the native variety, the other common varieties of
mangoes grown in Togo are: Kent, Palmer, Eldon and Somnole
(MAEDR 2020). Despite their economic and nutritional
importance, horticultural and mainly mango production and
trade are threatened by pests affecting the implementation
of the horticultural sector’s development policies. Of insect
pests attacking fruits and vegetables fruit flies (Diptera:
Tephritidae) ranked as being one of the most important eco-
nomically. The losses attributed to fruit flies in sub-Saharan
Africa have been increasing in recent years because, in addi-
tion to the indigenous species like Ceratitis cosyra (Walker)
(Diptera: Tephritidae) which attack fruits and reduce their
nutritional and trade values, a new species, Bactrocera dor-
salis (Hendel) (Diptera: Tephritidae) originated from South-
east Asia was first detected in Kenya in 2003, was introduced
from Southeast Asia (Pouillès-Duplaix 2008; Vayssières
et al. 2014). In a few years, this species has spread through-
out West Africa (Drew et al. 2005), as an invasive species.
B. dorsalis is economically very important because West
Africa is a favorable ecological niche for its development, in
terms of climate and availability of preferred host plants (De
Meyer 2010; Goergen et al. 2011; Gomina 2015). Being the
main species associated with the mango, B. dorsalis and C.
cosyra are the major constraints on mango production and
trade today. Mango losses caused by these major pests are
estimated at 17% at the beginning of the harvest period and
can exceed 70% at the end of the period (Vayssières et al.
2009a, b). As fruit flies are classified as “quarantine insects”,
any container from Africa containing perforated fruits is
intercepted, seized and destroyed by incineration at ports
and airports in Europe, causing serious economic losses
to African exporters (Pouillès-Duplaix 2008; Guichard
2009). Between 2006 and 2007, interceptions associated
with fruit flies increased by 23% and the annual economic
losses were estimated at more than USD 42 million in Africa
and more than one USD 1.0 billion worldwide (STDF 2009).
13
International Journal of Tropical Insect Science
For West Africa, interceptions related to fruit flies at the EU
border, cost around € 9,000,000 in mango exports in 2006
(ARAA 2018).
In order to reduce the level of fruit fly infestations below
economic thresholds in orchards and also, to avoid inter-
ceptions of fruits and vegetables in general and mangoes
in particular (from ECOWAS countries), the European
Union countries and eleven ECOWAS countries (Benin,
Ivory Coast, Burkina Faso, Gambia, Ghana, Guinea Cona-
kry, Mali, Nigeria, Senegal, Togo) have decided to combine
their efforts to control fruit flies. ECOWAS has therefore
initiated a sub-regional project entitled "Project to support
the regional plan for the control of fruit flies in West Africa
(PLMF)". One of the most important components of this
project is the accurate monitoring of fruit fly populations
for early warning and adequate decision-making for con-
trolling the pests in the interest of farmers. The study aimed
to: (i) present the state of diversity of fruit fly species in
different mango production areas in Togo and (ii) point out
the boundaries of the areas considered to be infested or free
from fruit flies by assessing the prevalence of species at the
beginning of the project. This is fundamental to develop-
ing accurate management methods, targeting the dominant
fruit fly species in the agro-ecosystems or mango producing
areas in Togo, and gathering a reference database to facili-
tate future assessment of the effectiveness of management
activities implemented in the country.
Materials and methods
Study area: geographic location, ecological
characteristics and choice of the orchards
The study was carried out in mango orchards in Togo, West
Africa. The study area extends from the South to the North
of this country, between 06.35964°N and 10.99362°N and
from East to West, between 000.31449°E and 001.29350°E.
A total of twenty orchards were chosen based on their areas
(minimum area of 2 ha); age (between 5 and 40 years); non-
application of phytosanitary measures and all the varieties
of mangoes identified (Fig. 1 and Table 1). The orchards
are geographically located in two of the five West African
mango producing belts recognized by the PLMF; one in the
South ­(TG1) or wet area and the other in the North ­(TG2) or
dry area. They are distributed in the five ecological zones of
Togo described by Ern (1979) and Brunel (1984) as follows:
– the North-East, North-West, Center and South-East of
ecological zone I (orchards T
­ G2V4, ­TG2V5, ­TG2V7 and
­TG2V10) or the northern plains with Sudan-savannas,
dry forests, meadows around ponds and agroforestry
parks. The climate is Sudano-tropical type with a sin-
International Journal of Tropical Insect Science

Fig. 1  Distribution of orchards under surveillance in ecological zones of Togo

13
 International Journal of Tropical Insect Science

Table 1  Description of orchards for surveillance of fruit flies in Togo

Orchard code* Location Orchard Age Area Mango varieties
(Village or Town) (years) (ha) in the orchard

TG1V1 Folli Kopé (Badja) 10 2 Pistolet, Somnole, Gouverneur, Smith, Eldon

TG1V2 Agou Wudralé 5 36 Somnole, Kent, Gouverneur, Pistolet, Palmer
TG1V3 Sognokopé (Namgbéto) 15 2 Smith
TG1V4 Agan (Est-Mono) 15 4 Somnole, Eldon, Smith
TG1V5 Babadè (Sotouboua) 23 2,5 Somnole, Kent, Davis, Palmer
TG1V6 Fédémé (Badja) 10 2 Pistolet, Gouverneur, Papaye
TG1V7 Agou Akplolo 40 3 Somnole, Palmer, Eldon, Smith, Kent, Hade, Bruce
TG1V8 Adjakpa (Amoussoukopé) 18 3 Somnole, Kent, Gouverneur, Pistolet, Palmer, sensation
TG1V9 Kériadè (Koumongou) 26 5 Eldon, Chinois
TG1V10 Watchalo (Sotouboua ville) 24 2 Smith, Eldon, Palmer, Somnole, Gouverneur, Valencia,
Aden, Davis, Bruce, Kent
TG2V1 Sada (Tchaoudjo) 15 25 Eldon, Smith, Kent
TG2V2 Tagbadè (Assoli) 10 4,5 Eldon, Pistolet, Smith, Somnole
TG2V3 Kpanzindè (Kozah) 25 3,5 Smith, Bruce, Kent, Sensation
TG2V4 Gando (Oti) 10 4 Pistolet, Smith, Gouverneur, etc
TG2V5 Samloaga (Kpendjal) 23 2 Smith, Bruce, Kent, Sensation
TG2V6 Pya (Akeyi) 40 3 Kent, Somnole
TG2V7 Kanté (Atè) 8 2 Pistolet, Gouverneur, Eldon, Kent, Palmer, Irwin
TG2V8 Kassena (Tchaoudjo) 18 2 Maloula, Francis, Somnole, Palmer, Pistolet, Sprint
Field, Kent, Davis
TG2V9 Sagbadaï (Sokodé) 18 2,25 Pistolet, Eldon, Gouverneur, Rubi, Kent, Somnole
TG2V10 Dapaong 39 3 Gouverneur, Alphonse, Davis, Zaïre
*
 TG1 Mango producing area, 1; T
­ G2 Mango producing area, 2; ­V1-V10 Orchard 1 to 10

gle rainy season (June-October) and a longer dry season
dominated by the harmattan (November–May). The aver-
age annual rainfall is around 1000 mm and the average
annual temperatures are generally high, reaching 28 °C
while relative humidity is low (53 to 67% RH);
– the North-East, Center and South of ecological zone
II (orchards ­TG1V5, ­TG1V9, ­TG1V10, ­TG2V2, ­TG2V3,
­TG2V6, ­TG2V8, ­TG2V9) or part of the Northern mountains
dominated by a mosaic of dry forests, mountain savan-
nas and crop lands. The climate is a Sudano-Guinean
type with one rainy season (April–October) and one dry
season (November to March), including the harmattan.
The temperature and relative humidity are closed to those
of Zone I;
– the South-East, Center and North-East of ecological
zone III (orchards T ­ G1V3, ­TG1V4, ­TG2V1,) or the cen-
tral plains made of woody Guinea-savannas, dry forests,
cropped lands as well as forest galleries. The climate of
the area is lowland Guinea-type, with one rainy season
(April to October) and one dry season (November to
March). The average annual temperatures vary between
26 and 30 °C while the average annual rainfall is around
1200 mm;
– the South-west of ecological zone IV (orchard ­TG1V7) or
the southern section of “mount Togo” dominated by Semi-
deciduous rainforest, cropped lands and Guinea-savannas.
It is influenced by a transition subequatorial climate, that
is, a mountain climate characterized by one rainy sea-
son (March-November) and one dry season (December-
February) with decreased rainfall in August. The average
monthly temperatures varied between 22 and 26 °C during
the year, the annual average rainfall is around 1,651 mm
and the relative humidity is always high (70 to 99% RH);
– the North-West and West of ecological zone V (orchards
­TG1V1, ­TG1V2, ­TG1V6, ­TG1V8) or the coastal plain of
Southern Togo characterized by Guinea-savannas, forest
patches, and cropped lands. Here there is a subequatorial
climate characterized by two rainy seasons (April-July
and September–October) alternating with two dry sea-
sons (August and November-March). Average monthly
temperatures vary between 25 and 28 °C during the year
and average annual rainfall is around 930 mm with a high
relative humidity throughout the year (73 to 90% RH).
Design of the Fruit fly capture device
The fruit fly traps were made with the aid of monitor-
ing traps using a dry bait or parapheromone specific to
males: Tephri Trap of the McPhail type (IAEA 2003). The

13
International Journal of Tropical Insect Science
parapheromones used have well known spectra (IAEA 2003;
Vayssières et al. 2004; FAO 2014)
and consist of: (i) Methyl Eugenol (ME) which attracts
mainly males of Bactrocera spp. and species of the subgenus
Ceratitis McLeay (Pardalaspis); (ii) Cue Lure (CUE) which
attracts mainly males of several species of the genus Dacus
and individuals of the Zeugodacus cucurbitae (Coquil-
lett) species; (iii) Terpinyl Acetate (TA) and (iv) Trimed-
lure (TM) which attract males of the genus Ceratitis. An
organophosphate chemical insecticide, DDVP or dichlor-
vos (2,2-dichlorovinyl dimethyl phosphate) was used to kill
entrapped flies. The parapheromones were renewed every
6 weeks and the chemical insecticide every two months
to maintain the effectiveness of the trap during the study
period (Gomina et al. 2012). The traps were installed in
the orchards from May 3 to June 8, 2018 according to the
fruit fly monitoring system set up by the PLMF. In effect, a
mango tree located at the center of each orchard was marked.
Around this central point, 4 other mango trees forming a
rhombus with sides 100 m and having as center the pre-
viously identified central point were also marked. On 4
mango trees located around each of these 4 points forming
the rhombus, 4 traps each containing a parapheromone were
installed: Methyl Eugenol, Cuelure, Tridmedlure and Terpi-
nyl Acetate traps with North, South, East and West orienta-
tion respectively. Sixteen traps were installed per orchard,
each with parapheromone, repeated 4 times. A total of 320
traps were installed for monitoring fruit flies in the selected
20 orchards. The traps were placed under the crown, shaded
by leaves 2 m from the ground. They were inspected during
a period of one month and 6 days started from ­3rd May to ­8th
June 2018. The collection of the traps’ catches of fruit flies
were carried out weekly from 2­ 5th May 2018. A total of 2
surveys were carried out in this period. Individuals of the
Tephritidae species captured were stored per type of para-
pheromone and orchard in 70% ethanol and transported to
the laboratory for identification.
Identification of fruit flies
The Tephritidae captured by each trap were sorted and iden-
tified at the Applied Entomology Laboratory (LEA) of the
University of Lomé, using dichotomous keys (De Meyer
1996; De Meyer 2000; White 2006; De Mayer and White
2008; Virgilio et al. 2014) and identification key leaflets of
the main fruit fly species in West Africa, provided by the
PLMF. Also, comparisons with the reference collection of
Tephritidae from LEA (samples of whose species have been
confirmed by the entomology section of the Royal Museum
for Central Africa (MRAC) in Tervuren in Belgium) were
made to revise the identification.
Data analysis
The trapped fruit flies were counted by species, orchard and
date of collection. The diversity of Tephritidae in orchards
was expressed in terms of alpha diversity (α) and beta diver-
sity (β). The calculations were done in R (R Core Team 2018)
with the entropart package (Marcon and Hérault 2015).
The α diversity is the number of species coexisting in a
uniform habitat of fixed size (Marcon 2015, 2018). It was
determined by the species richness or number of species of
fruit flies per orchard. The Simpson and Shannon–Wiener
diversity index as well as the Pielou evenness index that
often comes with the Shannon–Wiener index and Engen
rarity variance (EVS) (Marcon 2018) were estimated on
the basis of the Tephritidae samples from the catches. The
Simpson Index (SI) measures the probability that two ran-
domly selected individuals are of different species. It var-
ies from 0 to 1, diversity is highest for SI close to 1 and
lowest for SI close to 0. This diversity is also a decreas-
ing function of the regularity of the species. Considered a
measure of biodiversity as well as a quantitative measure,
the Shannon–Wiener index (H ’) varies from 0 (single
species, or one species dominates all the others) to log2
(S) (all species have the same abundance) where S is the
number of species. It is maximum when the frequencies
of the species encountered show little difference between
them. The Pielou evenness index (E) defines the regularity
of the distribution of species and corresponds to the ratio
of the Shannon index to its maximum value. It is close to
0 if the abundances of the species encountered are very
dissimilar and close to 1 if all the species have similar
abundance. The Engen rarity variance is the variance of
the information function, Shannon’s entropy. The closer
its value is to 0, the more equitable is the geographic area.
The beta diversity measures the difference or similarity
between habitats or samples in terms of species diversity. It
permits comparison of the diversity between the commu-
nities and was estimated by the Jaccard index (J) between
two orchards. The Jaccard index is 1 if there is complete
similarity between the localities compared and 0 if the latter
have no common species. A projection of the dissimilarity
matrix from the Jaccard indexes on the first main coordinates
made it possible to highlight similarities and dissimilarities
between the orchards in terms of diversity of fruit flies using
the R ade4 package (Bougeard and Dray 2018).
The analysis of the mean number and percentage of
fruit fly species was performed using analysis of variance
(ANOVA), followed by Student–Newman–Keuls (SNK)
comparison tests when the value of F was significant at
the 5% level.
The prevalence of the dominant fruit fly species was
determined by calculating the number of flies per trap
13

per day (FTD) according to IAEA (2003) and Rodríguez-
Rodríguez et  al. (Rodríguez-Rodríguez et  al. 2018),
applied in the case where no control measures were taken
in the orchards considered. According to IAEA (2003), the
value of FTD determines the type of phytosanitary meas-
ure to be considered in the implementation of international
standards for phytosanitary measures:
– if FTD˃1, the area is considered infested with fruit flies
and requires the full complement of phytosanitary meas-
ures;
– if 0.1 ≤ FDT ≤ 1, the actions to be taken are suppressing
the species of fruit fly;
– FDT ˂ 0.1 calls for an eradication process applied in an
area free from fruit flies;
– FTD = 0 calls for exclusion measures which are processes
applied to minimize the risk of introducing or reintroduc-
ing the species in an area free from fruit flies. Trapping
is applied to determine the presence of species that are
subject to exclusion measures and confirms or rejects the
status of a free zone.
Results
Alpha diversity
Species richness of fruit flies in the study area
A total of 40 species of Tephritidae were identified in the
five ecological zones based on the trap catches using the four
types of parapheromone (Table 2). Under the study condi-
tions, ecological zone II was the richest (36 species) while
ecological zone I the poorest (10 species). Ecological zones
III, IV and V recorded 25, 22 and 20 species respectively.
The species identified belong to three subfamilies (Daci-
nae, Tephritinae and Trypetinae) and 7 genera (Bactrocera
Macquart, Ceratitis McLeay, Celidodacus Hendel, Dacus
Fabricius, Elaphromyia Bigot, Trirhithrum Bezzi and Zeu-
godacus Hendel). The subfamilies Tephritinae and Trypeti-
nae were absent from ecological zones I, III, IV and V. The
genera Ceratitis and Dacus were the most diverse in species
with 17 and 14 species respectively. The other genera were
represented by one species only. Four Tephritidae are yet to
be precisely identified to the generic and species level.
The number of species caught per orchard varied from 4
(10% of the species) in the ­TG2V10 orchard to 26 (65% of the
species) in T
­ G2V2. The relatively more species-rich orchards
were found in ecological zones II, III and IV. The majority
of orchards, relatively poor in species were located above
latitude 09° 30′ 0′’ N, in the north of Togo in the ecological
zone I (Fig. 1).
13
International Journal of Tropical Insect Science
Species diversity of Tephritidae
During the survey, an average total number of 19,506.45
individuals of Tephritidae were caught per orchard, all
species combined. Out of this total number of fruit flies,
B. dorsalis represented in average 88.81% (17,546.50 indi-
viduals per orchard) and C. cosyra, 8.10% (1,598.95 indi-
viduals per orchard) (Table 3). The remaining 38 species
represented only 3.09% of the population of fruit flies per
orchard (361 individuals per orchard). Whether in zone 1
or zone 2, the mean numbers and proportions of B. dorsa-
lis and C. cosyra in the mango orchards were still higher
than other fruit fly species numbers (Table 3).
Analysis of the species diversity of Tephritidae showed
that the Simpson diversity indexes from the different
orchards were generally low, indicating a low diversity
of species (Table 4). These results are confirmed by the
low values of the Shannon–Wiener diversity indexes which
are well below the maximum value (Hmax). The Pielou
evenness index with relatively very low values correspond
to orchards T­ G1V9, ­TG1V10 and ­TG2V9 (Ecological Zone
II) and T
­ G 2V 5 (Ecological Zone I). The weak Simpson
index from these orchards indicated that they had a low
regularity of occurrence of the species. The distribution
of species in these orchards was marked by the dominance
of the B. dorsalis species.
Computation of the Engen rarity variance showed that
orchards ­TG1V2 and ­TG1V3 present the most homogeneous
sample distribution, while orchards T­ G2V5 (lower species
richness) and T­ G2V10 show the greatest disparities marked
by an unequal distribution of probabilities and low species
richness.
Beta diversity
Species community analysis of the Tephritidae species
showed that several orchards at the study site had similar
species because, the Jaccard index was higher than 0,50
(Table 5). The highest similarity was observed between
orchards ­TG1V5 and T ­ G2V9; ­TG1V7 and T­ G1V9; ­TG1V2
and ­TG1V6, with Jaccard indexes estimated at 0.94, 0.87
and 0.84, respectively. Orchards ­T G 1 V 7 and T ­ G 2V 4,
­TG1V9 and ­TG2V4 were those in which very low similar
species were recorded, with a Jaccard index of 0.13 each.
Bactrocera dorsalis, C. cosyra and C. fasciventris
were the three Tephritidae species that were present in
all the orchards studied (Table 1). They are followed by
C. capitata, D. humeralis and D. punctatifrons which
were present in 16 orchards and C. bremii, D. bivittatus
and Z. cucurbitae which were trapped in 15 orchards.
 Table 2  Presence of the Tephritidae species in different mango orchards in Togo*
Species TG1V1 TG1V2 TG1V3 TG1V4 TG1V5 TG1V6 TG1V7 TG1V8 TG1V9 TG1V10 TG2V1 TG2V2 TG2V3 TG2V4 TG2V5 TG2V6 TG2V7 TG2V8 TG2V9 TG2V10

Bactrocera dor-  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
salis (Hendel)
Celidodacus sp.  ×   × 
Ceratitis anonae  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
Graham
Ceratitis bremii  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
Guérin-
Méneville
Ceratitis capi-  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
tata (Wiede-
International Journal of Tropical Insect Science

mann)
Ceratitis colae  × 
Silvestri
Ceratitis cosyra  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
(Walker)
Ceratitis ditis-  ×   ×   ×   ×   ×   ×   × 
sima (Muro)
Ceratitis  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
fasciventris
(Bezzi)
Ceratitis flava  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
Meyer & Frei-
dberg
Ceratitis flexu-  × 
osa Walker
Ceratitis penicil-  ×   ×   ×   ×   ×   × 
lata Bigot
Ceratitis punc-  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
tata (Wiede-
mann)
Ceratitis qui-  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
naria Bezzi
Ceratitis silves-  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
trii Bezzi
Ceratitis sp1  ×   × 
Ceratitis sp2  ×   × 
Ceratitis sp3  × 
Ceratitis sp4  ×   ×   × 
Dacus armatus  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
Fabricius

13


Table 2  (continued)
Species TG1V1 TG1V2 TG1V3 TG1V4 TG1V5 TG1V6 TG1V7 TG1V8 TG1V9 TG1V10 TG2V1 TG2V2 TG2V3 TG2V4 TG2V5 TG2V6 TG2V7 TG2V8 TG2V9 TG2V10

13
Dacus bivittatus  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
(Bigot)
Dacus diastatus  ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
Munro
Dacus fuscovit-  ×   ×   ×   ×   ×   × 
tatus Graham
Dacus humeralis  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
(Bezzi)
Dacus langi  ×   ×   ×   ×   ×   ×   ×   ×   × 
Curran
Dacus mediovit-  ×   ×   ×   ×   ×   ×   ×   ×   × 
tatus White
Dacus punctati-  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
frons Karsch
Dacus theo-  ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
phrastus
Hering
Dacus guineen-  ×   ×   ×   × 
sis Hering
Dacus vertebra-  ×   ×   ×   ×   ×   ×   ×   × 
tus Bezzi
Dacus annulatus  × 
Becker
Dacus disjunctus  × 
(Bezzi)
Dacus seguyi  × 
(Munro)
Elaphromyia sp.  ×   × 
Tephritidae1  ×   × 
Tephritidae2  × 
Tephritidae3  × 
Tephritidae4  × 
Trirhithrum sp1  ×   × 
Zeugodacus  ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   ×   × 
cucurbitae
(Coquillett)
Species richness 12 18 16 19 17 18 22 16 21 21 24 26 21 5 6 8 8 22 16 4
*
 TG1 Mango producing area, 1; ­TG2 Mango producing area, 2; ­V1-V10 Orchard 1 to 10; × Presence of the species
International Journal of Tropical Insect Science
International Journal of Tropical Insect Science

Table 3  Mean number and proportion of the Tephritidae species per orchard (mean ± Std. Error) in different mango producing areas
Species/Statistics Average number of the species per orchard (Average proportion per orchard) *
Zone 1 (TG1)** Zone 2 (TG2)** All zones (TG)**

B. dorsalis 21,069.40 ± 6,383.08a (91.31 ± 2.00a) 14,023.60 ± 4,492.80a (82.10 ± 5.26a) 17,546.50 ± 3,883.78a (88.81 ± 1.73a)

C. cosyra 1,766.60 ± 1,123.80b (4.88 ± 2.22b) 1,431.30 ± 495.00b (15.24 ± 4.70b) 1,598.95 ± 598.85b (8.10 ± 1.66b)
D. armatus 176.40 ± 152.15c (0.71 ± 0.25c) 1.20 ± 0.99 (0.00 ± 0.02c) 88.80 ± 76.73b (0.36 ± 0.15c)
D. humeralis 113.40 ± 46.51c (0.46 ± 0.11c) 63.10 ± 32.79 (0.21 ± 0.08c) 88.25 ± 28.29b (0.33 ± 0.07c)
C. fasciventris 16.80 ± 5.45c (0.36 ± 0.19c) 97.70 ± 57.19 (0.82 ± 0.38c) 57.25 ± 29.46b (0.60 ± 0.22c)
C. capitata 45.30 ± 24.10c (0.83 ± 0.40c) 6.90 ± 5.49 (0.03 ± 0.02c) 26.10 ± 12.81b (0.43 ± 0.21c)
D. bivittatus 38.70 ± 15.67c (0.28 ± 0.31c) 9.20 ± 3.97 (0.04 ± 0.02c) 23.95 ± 8.57b (0.16 ± 0.06c)
D. theophratus 21.70 ± 17.65c (0.06 ± 0.05c) 2.10 ± 0.94 (0.01 ± 0.00c) 11.90 ± 8.89b (0.03 ± 0.02c)
Z. cucurbitae 14.00 ± 5.98c (0.27 ± 0.13c) 4.00 ± 2.08 (0.02 ± 0.01c) 9.00 ± 3.29b (0.14 ± 0.07c)
C. silvestrii 4.00 ± 2.59c (0.01 ± 0.01c) 9.60 ± 2.39 (0.73 ± 0.47c) 6.80 ± 1.83b (0.33 ± 0.23c)
C. anonae 11.50 ± 8.27c (0.08 ± 0.04c) 0.60 ± 0.27 (0.00 ± 0.00c) 6.05 ± 4.22b (0.04 ± 0.02c)
Ceratitis sp2 11.70 ± 10.74c (0.20 ± 0.16c) 0.00 ± 0.00 (0.00 ± 0.00c) 5.85 ± 5.49b (0.10 ± 0.08c)
C. quinaria 2.60 ± 1.92c (0.01 ± 0.00c) 8.30 ± 1.99 (0.54 ± 0.28c) 5.45 ± 1.50b (0.22 ± 0.13c)
C. bremii 3.30 ± 2.03c (0.02 ± 0.01c) 6.90 ± 2.55 (0.15 ± 0.08c) 5.10 ± 1.64b (0.05 ± 0.02c)
D. punctatifrons 8.50 ± 2.13c (0.18 ± 0.06c) 1.00 ± 0.39 (0.00 ± 0.00c) 4.75 ± 1.36b (0.09 ± 0.04c)
D. diastatus 4.50 ± 1.93c (0.01 ± 0.00c) 1.90 ± 0.89 (0.01 ± 0.00c) 3.20 ± 1.08b (0.01 ± 0.00c)
C. penicillata 5.50 ± 3.62c (0.05 ± 0.02c) 0.30 ± 0.30 (0.00 ± 0.00c) 2.90 ± 1.87b (0.02 ± 0.01c)
D. mediovittatus 5.20 ± 1.53c (0.13 ± 0.06c) 0.30 ± 0.30 (0.00 ± 0.00c) 2.75 ± 0.94b (0.07 ± 0.03c)
C. ditissima 1.50 ± 0.78c (0.04 ± 0.03c) 3.20 ± 2.36 (0.01 ± 0.01c) 2.35 ± 1.22b (0.02 ± 0.01c)
Other species 11.30 ± 5.16c (0.11 ± 0.04c) 9.80 ± 5.21 (0.09 ± 0.05c) 10.55 ± 3.57b (0.09 ± 0.01c)
Total 23,332 (100) 15,681 (100) 19,506.45 (100)
F 10.52 893.06 9.60 136 19.86 1316.39
df 19 19 19 19 19 19
p 0.00 0.00 0.00 0.00 0.00 0.00
*
 In the same colon, means followed by a different letter are significantly different (ANOVA-1 followed by SNK test, P < 0.05)
**
 TG1: Mango producing area 1; ­TG2: Mango producing area 2; TG: Total orchards in the study area; Number of replications: 10 per zone ­(TG1
or ­TG2) and 20 in the study area (TG)

The uncommon species that were present in only one orchard
were C. colae ­(TG1V7), C. flexuosa ­(TG1V10), Ceratitis
sp3 ­( TG 2V 2), D. annulatus ­( TG 2V 1), Dacus disjunctus
(Bezzi) ­( TG 1V 9), Dacus seguyi (Munro) (­ TG 2V 2) and
unidentified Tephritidae 2, 3 and 4 that were recorded in
orchards ­TG2V3, ­TG2V2, respectively.
The representation of the orchards in the different
zones in a principal coordinate analysis based on the Jac-
card distances allowed to better group the orchards having
similar species (Fig. 2). Four main groups of orchards were
identified:
– group 1 comprised orchards T ­ G1V4, ­TG1V5, ­TG2V1,
­TG2V2, ­TG2V3, ­TG2V8 and T ­ G2V9 that had more than
half of the species similar;
– group 2 are orchards T ­ G1V1, ­TG1V8, ­TG1V2, ­TG1V6,
which also had more than half of the species similar;
– group 3 includes orchards ­TG1V3, ­TG1V7 and ­TG1V9
which were similar;
– group 4: orchards ­TG2V4, ­TG2V6 and ­TG2V7;
Orchards ­TG2V5, ­TG2V10 and ­TG1V10 were not well rep-
resented in the projection made.
Species prevalence
Based on species diversity, B. dorsalis and C. cosyra were
common to all the mango orchards in the study area and
singly represented 98.15% of the Tephritidae. Indeed, the
number of flies per trap per day (FTD) of B. dorsalis was
the highest in all the orchards and varies from 2.12 ­(TG2V4)
to 472.1 (­ TG1V7) (Fig. 3). The prevalence of C. cosyra was
lower and ranged between 0.34 ­(TG2V4) and 97.28 ­(TG1V4).
Discussion
The trap-capture method used in this study made it possible
to record 40 species of Tephritidae, 11 of which were not be
identified up to species level. Those identified represent 77%

13
 International Journal of Tropical Insect Science

Table 4  Alpha diversity index Orchardcode* Simpson diversity Shannon Wiener Maximum Pielou evenness Engen rarity
of Tephritidae in mango index (D) diversity index (H’) diversity index (E) variance (EVS)
orchards of Togo (Hmax)

TG1V1 0.122 0.503 3.584 0.140 2.596

TG1V2 0.158 0.690 4.169 0.165 3.661
TG1V3 0.183 0.761 4.000 0.190 3.630
TG1V4 0.382 0.882 4.247 0.216 1.092
TG1V5 0.104 0.342 4.087 0.084 1.337
TG1V6 0.215 0.844 4.169 0.206 3.628
TG1V7 0.131 0.502 4.459 0.113 2.344
TG1V8 0.100 0.439 4.000 0.112 2.536
TG1V9 0.089 0.349 4.392 0.079 1.776
TG1V10 0.070 0.269 4.392 0.061 1.399
TG2V1 0.202 0.572 4.584 0.125 1.550
TG2V2 0.182 0.599 4.700 0.127 2.244
TG2V3 0.448 1.135 4.392 0.258 1.642
TG2V4 0.396 1.133 2.321 0.488 2.036
TG2V5 0.047 0.179 2.584 0.069 0.882
TG2V6 0.284 0.806 3.000 0.269 1.958
TG2V7 0.546 1.366 3.000 0.455 1.560
TG2V8 0.171 0.513 4.459 0.115 1.642
TG2V9 0.092 0.328 4.000 0.082 1.478
TG2V10 0.207 0.540 2.00 0.270 1.079
*
 TG1: Mango producing area 1; T
­ G2 : Mango producing area 2; V
­ 1-V10 : Orchard 1 to 10

of the species reported in Togo and 34.2% of those in West
Africa (De Meyer 2005; De Meyer et al. 2013). The flies
identified up to species level were those of the Dacinae sub-
family reported in Togo and other countries of the afrotropi-
cal region (Amevoin 2009; Ouédraogo et al. 2011; Gomina
et al. 2012; De Meyer et al. 2013; N’Da 2018; Zida et al.
2020). The relatively high species richness obtained with
a single study method applied over a month is an evidence
that the species found in the mango orchards (which were
at fruit ripening stage) and their surrounding vegetation, a
favorable abiotic (temperature, relative humidity, precipita-
tion, etc.) and biotic (resting sites, host plants) conditions for
their development (Virgilio et al. 2009; Goergen et al. 2011,
Bota et al. 2020). These may explain the diversification in
species of the two main genera Ceratitis and Dacus. Indeed,
Vayssières et al. (2010) and Gomina (2015) reported the
presence of the host plants of several Tephritidae species
identified in this study. The highest species richness was
observed in the ecological zones II, III (at the level of the
latitude of Sokodé and Bafilo) and IV. This can be explained
not only by the diversification level of wild host plants but
especially by the fruit trees cultivated in these areas. In fact,
the zones II, III and IV are considered in Togo as major fruit
producing regions, which is not the case for the ecological
zone I in the Northern part of the country where the diversity
of host plants may be lower, probably because of the less
favorable ecological and climatic conditions. Similar study
conducted by Bota et al. (2020) also showed that the popu-
lation of fruit flies that infest mango orchards in the central
Mozambique may come from the marginal area, especially
from local varieties of mango which get matured earlier.
Among the species of Tephritidae identified in mango
orchards in Togo, B. dorsalis, C. cosyra, C. capitata, C.
fasciventris, C. silvestrii, C. anonae, C. quinaria, C. ditis-
sima are known to be associated with various fruit plant
species in Africa (Vayssières et al. 2004; White and Elson-
Harris 1992; Vayssières et al. 2009a, b; Nboyine et al. 2013;
Vayssières et al. 2015; Zida et al. 2020). According to Vays-
sières et al. (2015) the presence of several fruit fly species
on mango has considerably reduced the potential economic
benefits of growing this fruit tree in West Africa. As for
the Tephritidae species of the genera Dacus and Zeugoda-
cus, they are known to attack mostly plant species belong
to Cucurbitaceae, Passifloraceae and Apocynaceae (White
2006; Virgilio et al. 2009). In general, the mango fruit flies
identified during our study are native, except of B. dorsalis
and Z. cucurbitae reported as exotic and invasive (Goergen
et al. 2011; De Meyer et al. 2013).
The very high proportions and prevalence of B. dorsalis
in all the mango orchards in Togo is an evidence that this
invasive species has settled in Togo and has undoubtedly
constituted a threat to mango and other fruits production.

13
 Table 5  Jaccard indices from the different mango orchards in the study area
TG1V10 TG1V2 TG1V3 TG1V4 TG1V5 TG1V6 TG1V7 TG1V8 TG1V9 TG2V1 TG2V10 TG2V2 TG2V3 TG2V4 TG2V5 TG2V6 TG2V7 TG2V8 TG2V9

TG1V1 0.43 0.58 0.56 0.45 0.45 0.71 0.48 0.69 0.50 0.44 0.23 0.27 0.38 0.21 0.38 0.25 0.18 0.42 0.47
International Journal of Tropical Insect Science

TG1V10 0.56 0.61 0.58 0.73 0.58 0.65 0.50 0.68 0.67 0.19 0.62 0.62 0.18 0.29 0.32 0.32 0.79 0.68
TG1V2 0.70 0.40 0.46 0.84 0.74 0.74 0.70 0.45 0.16 0.38 0.34 0.15 0.26 0.24 0.18 0.48 0.48
TG1V3 0.57 0.65 0.65 0.65 0.72 0.68 0.60 0.25 0.45 0.48 0.24 0.38 0.41 0.33 0.65 0.68
TG1V4 0.79 0.42 0.56 0.45 0.58 0.71 0.24 0.43 0.58 0.29 0.35 0.47 0.47 0.63 0.74
TG1V5 0.42 0.56 0.45 0.58 0.71 0.24 0.54 0.65 0.29 0.35 0.47 0.47 0.77 0.94
TG1V6 0.63 0.78 0.65 0.46 0.17 0.39 0.41 0.16 0.28 0.25 0.19 0.50 0.43
TG1V7 0.61 0.87 0.59 0.18 0.45 0.43 0.13 0.27 0.25 0.20 0.57 0.58
TG1V8 0.64 0.44 0.19 0.32 0.44 0.18 0.31 0.28 0.21 0.48 0.48
TG1V9 0.61 0.19 0.47 0.45 0.13 0.29 0.26 0.21 0.59 0.61
TG2V1 0.17 0.56 0.67 0.21 0.25 0.33 0.33 0.77 0.67
TG2V10 0.15 0.19 0.50 0.67 0.50 0.50 0.18 0.25
TG2V2 0.62 0.19 0.19 0.31 0.31 0.66 0.50
TG2V3 0.24 0.29 0.38 0.38 0.65 0.61
TG2V4 0.38 0.63 0.63 0.23 0.31
TG2V5 0.40 0.40 0.27 0.38
TG2V6 0.78 0.36 0.50
TG2V7 0.36 0.41
TG2V8 0.73

Index of the orchards hosting the greatest number of common species

13

Fig. 2  Graphic representation groups of mango orchards in a principal coordinate analysis based on Jaccard distances between the number of
fruit fly species
This result confirms the economic importance of B. dorsa-
lis reported in several African countries (Bota et al. 2018,
2020; N’Da 2018; Zida et al. 2020). The high proportion and
prevalence of B. dorsalis in mango orchards do not seem to
be explained solely by the effectiveness of the attractant used
for this species but mainly by its very good adaptation to the
agro-ecological conditions of the study area. In addition to
being polyphagous, Gomina (2015) has shown that under
the Guinea zone conditions in Togo, B. dorsalis was very
prolific because the female could lay an average of 538 eggs
during its life time with an offspring survival rate estimated
at 67%. C. cosyra is the second most important species to
which special attention must be paid in Togo and in West
Africa (Ouédraogo et al. 2011; Zida et al. 2020). This spe-
cies was considered as adapted to Sahelian and Sudanese
zones and absent from agro-ecological zones of the humid
forests of West Africa (Vayssières et al. 2014). However, it
was found in all ecological zones of the study area in Togo
13
International Journal of Tropical Insect Science
including zone IV dominated by dense semi-deciduous for-
ests. The presence of C. cosyra in the humid forest zone
in Togo is probably due to human activities which nega-
tively impact ecological zone IV and climate change with
its proven consequences in recent years.
The species richness of Tephritidae frugivores in Togo
seems to be important but the different diversity indexes
pointed out a low species diversity. This helps to note that
the potential species diversity in Tephritidae should be high.
This result is in line with the work of De Meyer et al. (2013).
Thus, the application of other methods such as the incuba-
tion of fruits from different ecological zones and the use of
other attractants will probably make it possible to accurately
record all species present in Togo.
Analysis of the Tephritidae community from the catches
shows that several fruit fly species that attack the mango
orchards studied were similar. The Jaccard distances analy-
sis showed that orchards in the same ecological zone tend
International Journal of Tropical Insect Science

500
480 B. dorsalis Conclusion
460 C. cosyra
440
420 This study confirms that there is no area that is free from
400 fruit flies in Togo. A total of 40 species of fruit flies were
380
360 identified in the surveyed mango orchards that were at fruit
340
maturation period. The diversity indexes estimated in this
FTD (flies/trap/day)

320
300 study show that species other than those reported in the
280
260 study could be present. The most common species are B.
240
220 dorsalis, C. cosyra, C. fasciventris, C. capitata, D. humer-
200
180 alis and D. punctatifrons, C. bremii, D. bivittatus and Z.
160 cucurbitae. The most abundant of these are the invasive
140
120 B. dorsalis and the endogenous C. cosyra which have a
100
80 very high prevalence. Hence, it is essential to determine,
60 in all agro-ecological zones, the economic thresholds of
40
20 these most abundant fruit flies (B. dorsalis and C. cosyra)
0
of the economically important fruits and vegetables. This
TG1V1
TG1V2
TG1V3
TG1V4
TG1V5
TG1V6
TG1V7
TG1V8
TG1V9
TG1V10
TG2V1
TG2V2
TG2V3
TG2V4
TG2V5
TG2V6
TG2V7
TG2V8
TG2V9
TG2V10
will lead to the establishment of a sustainable fruit flies
Orchards management program in Togo.

Fig. 3  Prevalence variation of the two major fruit fly species in the
mango orchards during the first month of monitoring
to be similar in terms of the fruit fly species present. This
result may indicate the homogeneity of the abiotic and biotic
conditions (the vegetation in particular represented by the
host plants cultivated inside the orchard but also by the wild
host plants around the latter) in the same zone allowing the
species of Tephritidae to find the same resources for their
survival and development. This result is similar to the one of
Ouédraogo et al. (2011). The most common and wide-ranging
species in our study area were B. dorsalis, C. cosyra, C.
fasciventris, C. capitata, D. humeralis and D. punctatifrons,
C. bremii, D. bivittatus and Z. cucurbitae. These species
are known to be well represented in West Africa (Gomina
et al. 2012; De Meyer et al. 2013; Ouédraogo et al. 2011;
Vayssières et al. 2015). The species C. colae, C. flexuosa,
Ceratitis sp and some species of the genus Dacus that were
not be identified up to the species level were present in a
single orchard and can probably be considered as being rare
in the area but, monitoring over a long period will make it
possible to confirm their status.
The prevalence of the two species considered dominant
in terms of number of flies per trap per day (FTD) is very
high and therefore indicates that all the orchards studied have
very high incidence of B. dorsalis and C. cosyra. Thus, they
remain the species of economic importance in Togo. Accord-
ing to the recommendations of IAEA (2003), this result indi-
cates that it is necessary to implement phytosanitary protec-
tion actions against these formidable species of fruit flies.
Acknowledgement  This study was carried out with the financial sup-
port of the European Union (EU), Agence Française de Développe-
ment (AFD) and the Economic Community of West African States
(ECOWAS) through the Support Project to the Regional Plan for the
Control of Fruit Flies in West Africa (PLMF). We thank all the staff
of the SOGEROM–COLEACP–BERD consortium who ensured the
regional coordination of the project. Additional financial support was
also provided by CABIs Plantwise Plus programme. Plantwise Plus
is supported by the UK Foreign, Commonwealth and Development
Office (FCDO), Netherlands Directorate General for International
Cooperation (DGIS), European Commission Directorate-General for
International Cooperation and Development (DEVCO) and the Swiss
Agency for Development and Cooperation (SDC). We also thank the
staff of “Direction de la Protection des Végétaux” of Togo, which was
responsible for coordinating the implementation of this project in Togo,
and all owners of mango orchards and technicians responsible for col-
lecting flies in the field, their counting and identification in the labora-
tory. Our thanks also go to Mr. Komlavi Yves Amevoin, Economic
Statistician at Médecins Sans Frontières (Dakar) for his invaluable help
in the statistical analysis of data as well as to Dr. Hodabalo Pereki
(Département de Botanique de la Faculté des Sciences de l’Université
de Lomé) for his contribution to mapping the study area and Dr Victor
Clottey (CABI, Ghana) and Dr Tetevi Wilson-Bahun (Faculté des
Sciences de l’Université de Lomé) for their contribution to improve
the English language.
Authors’ contributions  Data collection, K.A., L.K.A., K.K., K.H.B.,
M.D. and A.V.D., morphological identifications, M.G. and K.A. writ-
ing-original draft preparation, K.A. and L.K.A., writing-review and
editing, L.K.A., M.G. and K.A., Project administration, A.T. & K.H.B.
Funding  This study was carried out with the financial support of the
European Union (EU), Agence Française de Développement (AFD)
and the Economic Community of West African States (ECOWAS)
through the Support Project to the Regional Plan for the Control of
Fruit Flies in West Africa (PLMF). Additional financial support was
also provided by CABIs Plantwise Plus programme. Plantwise Plus is

13

supported by the UK Foreign, Commonwealth and Development Office
(FCDO), Netherlands Directorate General for International Coopera-
tion (DGIS), European Commission Directorate-General for Interna-
tional Cooperation and Development (DEVCO) and the Swiss Agency
for Developmentand Cooperation (SDC).
Data Availability  All data are available and insect specimens are con-
served in laboratory.
Declarations  mology 21: 15–26. https://​onlin​elibr​ary.​wiley.​com/​doi/​abs/​10.​
Conflicts of interest  The authors declare no conflict of interest.
Open Access  This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article’s Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article’s Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/.
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